Longitudinal Evidence for Attenuated Local-Global Deviance Detection as a Precursor of Working Memory Decline.

From the perspective of predictive coding, normal aging is accompanied by decreased weighting of sensory inputs and increased reliance on predictions, resulting in the attenuation of prediction errors in older age. Recent electroencephalography (EEG) research further revealed that the age-related shift from sensorium to predictions is hierarchy-selective, as older brains show little reduction in lower-level but significant suppression in higher-level prediction errors. Moreover, the disrupted propagation of prediction errors from the lower-level to the higher-level seems to be linked to deficient maintenance of information in working memory. However, it is unclear whether the hierarchical predictive processing continues to decline with advancing age as working memory. Here, we longitudinally followed a sample of 78 participants from three age groups (including seniors, adults, and adolescents) over three years' time. Seniors exhibited largely preserved local processing [consisting of comparable mismatch negativity (MMN), delayed P3a, and comparable reorienting negativity (RON)] but significantly compromised global processing (consisting of suppressed frontocentral negativity and suppressed P3b) in the auditory local-global paradigm. These electrophysiological responses did not change with the passing of time, unlike working memory which deteriorated with advancing age. Correlation analysis further showed that these electrophysiological responses signaling prediction errors are indicative of concurrent working memory. Moreover, there was a correlation between earlier predictive processing and later working memory but not between earlier working memory and later predictive processing. The temporal asymmetry suggested that the hierarchy-selective attenuation of prediction errors is likely a precursor of working memory decline.

The mismatch negativity to abstract relationship of tone pairs is independent of attention.

The mismatch negativity (MMN) implicating a comparison process between the deviant and the memory trace of the standard can be elicited by not only changes in physical features but also violations of abstract patterns. It is considered pre-attentive, yet the use of the passive design makes it difficult to exclude the possibility of attention leak. In contrast to how this issue has been well addressed with the MMN to physical changes, much less research directly investigated the attentional effect on the MMN to abstract relationships. Here we conducted an electroencephalography (EEG) experiment to study whether and how the MMN to abstract relationships is modulated by attention. We adapted the oddball paradigm of Kujala et al. by presenting occasional descending tone pairs among frequent ascending tone pairs, while additionally implementing a novel control of attention. Participants' attention was either directed away from the sounds (with an engaging task of visual target detection, so that the sounds were task-irrelevant) or toward the sounds (with a conventional task of auditory deviant detection, so that the sounds were task-relevant). The MMN to abstract relationships appeared regardless of attention, confirming the pre-attentive assumption. The attention-independence of the frontocentral and supratemporal components of the MMN supported the notion that attention is not required to generate the MMN. At the individual level, a relatively equal number of participants showed attention enhancement and attention suppression. It is unlike the attentional modulation on the P3b, which was robustly elicited in the attended condition only. The concurrent collection of these two neurophysiological markers in both unattended and attended conditions might be potentially suitable for testing clinical populations showing heterogeneous deficits in auditory function independent/dependent of attention.

Intention-based and sensory-based predictions.

We inhabit a continuously changing world, where the ability to anticipate future states of the environment is critical for adaptation. Anticipation can be achieved by learning about the causal or temporal relationship between sensory events, as well as by learning to act on the environment to produce an intended effect. Together, sensory-based and intention-based predictions provide the flexibility needed to successfully adapt. Yet it is currently unknown whether the two sources of information are processed independently to form separate predictions, or are combined into a common prediction. To investigate this, we ran an experiment in which the final tone of two possible four-tone sequences could be predicted from the preceding tones in the sequence and/or from the participants' intention to trigger that final tone. This tone could be congruent with both sensory-based and intention-based predictions, incongruent with both, or congruent with one while incongruent with the other. Trials where predictions were incongruent with each other yielded similar prediction error responses irrespectively of the violated prediction, indicating that both predictions were formulated and coexisted simultaneously. The violation of intention-based predictions yielded late additional error responses, suggesting that those violations underwent further differential processing which the violations of sensory-based predictions did not receive.

Attention modulates repetition effects in a context of low periodicity.

Stimulus repetition can result in a reduction in neural responses (i.e., repetition suppression) in neuroimaging studies. Predictive coding models of perception postulate that this phenomenon largely reflects the top-down attenuation of prediction errors. Electroencephalography research further demonstrated that repetition effects consist of sequentially ordered attention-independent and attention-dependent components in a context of high periodicity. However, the statistical structure of our auditory environment is richer than that of a fixed pattern. It remains unclear if the attentional modulation of repetition effects can be generalised to a setting which better represents the nature of our auditory environment. Here we used electroencephalography to investigate whether the attention-independent and attention-dependent components of repetition effects previously described in the auditory modality remain in a context of low periodicity where temporary disruption might be absent/present. Participants were presented with repetition trains of various lengths, with/without temporary disruptions. We found attention-independent and attention-dependent repetition effects on, respectively, the P2 and P3a event-related potential components. This pattern of results is in line with previous research, confirming that the attenuation of prediction errors upon stimulus repetition is first registered regardless of attentional state before further attenuation of attended but not unattended prediction errors takes place. However, unlike previous reports, these effects manifested on later components. This divergence from previous studies is discussed in terms of the possible contribution of contextual factors.

Human Brain Ages With Hierarchy-Selective Attenuation of Prediction Errors.

From the perspective of predictive coding, our brain embodies a hierarchical generative model to realize perception, which proactively predicts the statistical structure of sensory inputs. How are these predictive processes modified as we age? Recent research suggested that aging leads to decreased weighting of sensory inputs and increased reliance on predictions. Here we investigated whether this age-related shift from sensorium to predictions occurs at all levels of hierarchical message passing. We recorded the electroencephalography responses with an auditory local-global paradigm in a cohort of 108 healthy participants from 3 groups: seniors, adults, and adolescents. The detection of local deviancy seems largely preserved in older individuals at earlier latency (including the mismatch negativity followed by the P3a but not the reorienting negativity). In contrast, the detection of global deviancy is clearly compromised in older individuals, as they showed worse task performance and attenuated P3b. Our findings demonstrate that older brains show little decline in sensory (i.e., first-order) prediction errors but significant diminution in contextual (i.e., second-order) prediction errors. Age-related deficient maintenance of auditory information in working memory might affect whether and how lower-level prediction errors propagate to the higher level.

The auditory N1 suppression rebounds as prediction persists over time.

The predictive coding model of perception proposes that neuronal responses reflect prediction errors. Repeated as well as predicted stimuli trigger suppressed neuronal responses because they are associated with reduced prediction errors. However, many predictable events in our environment are not isolated but sequential, yet there is little empirical evidence documenting how suppressed neuronal responses reflecting reduced prediction errors change in the course of a predictable sequence of events. Here we conceived an auditory electroencephalography (EEG) experiment where prediction persists over series of four tones to allow for the delineation of the dynamics of the suppressed neuronal responses. It is possible that neuronal responses might decrease for the initial predictable stimuli and stay at the same level across the rest of the sequence, suggesting that they reflect the predictability of the stimuli in terms of mere probability. Alternatively, neuronal responses might decrease for the initial predictable stimuli and gradually recover across the rest of the sequence, suggesting that factors other than mere probability have to be considered in order to account for the way prediction is implemented in the brain. We found that initial presentation of the predictable stimuli was associated with suppression of the auditory N1. Further presentation of the predictable stimuli was associated with a rebound of the component's amplitude. Moreover, such pattern was independent of attention. The findings suggest that auditory N1 suppression reflecting reduced prediction errors is a transient phenomenon that can be modulated by multiple factors.

Distinctive Representation of Mispredicted and Unpredicted Prediction Errors in Human Electroencephalography.

The predictive coding model of perception proposes that neuronal responses are modulated by the amount of sensory input that the internal prediction cannot account for (i.e., prediction error). However, there is little consensus on what constitutes nonpredicted stimuli. Conceptually, whereas mispredicted stimuli may induce both prediction error generated by prediction that is not perceived and prediction error generated by sensory input that is not anticipated, unpredicted stimuli involves no top-down, only bottom-up, propagation of information in the system. Here, we examined the possibility that the processing of mispredicted and unpredicted stimuli are dissociable at the neurophysiological level using human electroencephalography. We presented participants with sets of five tones in which the frequency of the fifth tones was predicted, mispredicted, or unpredicted. Participants were required to press a key when they detected a softer fifth tone to maintain their attention. We found that mispredicted and unpredicted stimuli are associated with different amount of cortical activity, probably reflecting differences in prediction error. Moreover, relative to predicted stimuli, the mispredicted prediction error manifested as neuronal enhancement and the unpredicted prediction error manifested as neuronal attenuation on the N1 event-related potential component. These results highlight the importance of differentiating between the two nonpredicted stimuli in theoretical work on predictive coding.

Repetition suppression comprises both attention-independent and attention-dependent processes.

Repetition suppression, a robust phenomenon of reduction in neural responses to stimulus repetition, is suggested to consist of a combination of bottom-up adaptation and top-down prediction effects. However, there is little consensus on how repetition suppression is related to attention in functional magnetic resonance imaging (fMRI) studies. It is probably because fMRI integrates neural activity related to adaptation and prediction effects, which are respectively attention-independent and attention-dependent. Here we orthogonally manipulated stimulus repetition and attention in a target detection task while participants' electroencephalography (EEG) was recorded. In Experiment 1, we found a significant repetition effect on N1 amplitude regardless of attention, whereas the repetition effect on P2 amplitude was attention-dependent. In Experiment 2 where the attentional manipulation was more stringent than that in Experiment 1, we replicated a significant repetition effect on N1 amplitude regardless of attention, whereas the repetition effect on P2 amplitude was eliminated. The results show that repetition suppression comprises both attention-independent and attention-dependent components.

Temporal expectation and spectral expectation operate in distinct fashion on neuronal populations.

The formation of temporal expectation (i.e., the prediction of "when") is of prime importance to sensory processing. It can modulate sensory processing at early processing stages probably via the entrainment of low-frequency neuronal oscillations in the brain. However, sensory predictions involve not only temporal expectation but also spectral expectation (i.e., the prediction of "what"). Here we investigated how temporal expectation may interrelate with spectral expectation by explicitly setting up temporal expectation and spectral expectation in a target detection task. We found that reaction time (RT) was shorter when targets were temporally expected than when they were temporally unexpected. The temporal expectation effect was larger with than without spectral expectation. However, this interaction in the behavioural data did not result from an interaction in the electroencephalography (EEG), where we observed independent main effects of temporal expectation and spectral expectation. More precisely, we found that the N1 and P2 event-related potential (ERP) components and the entrainment of low-frequency neuronal oscillations were exclusively modulated by temporal expectation, whilst only the P3 ERP component was modulated by spectral expectation. Our results, thus, support the idea that temporal expectation and spectral expectation operate in distinct fashion on neuronal populations.